A Survey of Tropical Ea.rthworms: Taxonomy, Biogeography and Environmental Plasticity 3 Carlos Fragoso\ Jean Kanyonyo2, Ana Moreno , 4 5 Bikram K. Senapati , Eric Blanchart and Carlos Rodriguez6

l Departamento Bi%gfa de Sue/os, Instituto de Ec%gfa, Xa/apa, Mexico; 2 Université du Rwanda, Butare, Rwanda; 3 Universidad Comp/utense, Madrid, Spain; 4Schoo/ of Life Sciences, Samba/pur University, Samba/pur, India; 5 Laboratoire B.O.s. T., IRD, Fort-de-France, Martinique; 6Universidad de /a Habana, La Habana, Cuba

Summary

A worldwide survey of earthworms in the humid tropics revealed that 51 exotics and 151 native species are commonly found in tropical agroecosystems. On the basis of frequency records and climatic and edaphic ranges, 21 exotics and 27 native species have been selected as possible candi­ dates for manipulation. A multivariate analysis separated these species into four groups: (i) native species with wide edaphic and medium climatic toler­ ances; (ii) exotic species with wide climatic and edaphic tolerances; (iii) native and exotic species with narrow edaphic tolerances but more resistant to climatic variations; and (iv) native species with limited tolerance for climatic and edaphic variations. Regarding management, species of group (ii) seem to be the most adapt­ able. both at regional and locallevels (multipurpose species); group (i) can be managed for specific climatic conditions whereas group (iii) should be managed in specific soil environments. Species of group (iv) may only be managed at a very local scale.

©CAB International 1999. Earthworm Management in Tropical Agroecosystems (eds P. Lavelle, L. Brussaard and P. Hendrix) 2 C. Fragoso et al.

Introduction

Earthworms are confmed to the soil and, for the majority of tropical farmers and agronomists, their diversity, activities and eiTects on soils are totally unknown. Even in the field of tropical soil science, the situation is not very dif­ ferent. For example, just a few years ago, there was little concern about earth­ worm diversity and the possible role of this diversity in the fertility of agroecosystems. During the last 10 years, however, there has been an increas­ ing interest in diversity mainly due to the biodiversity crisis, which could be defined as the dramatic loss of species, habitats and ecological interactions (Wilson, 1985; Wilson and Peter, 1988; McNelly et al., 1990). Although the most diverse tropical biota are insects that spend part of their life cycles in the sail, this environment has been, from a biodiversity viewpoint, one orthe least studied. Earthworms are not very diverse, and our current estimations of the number of existing species are far from complete. The most recent account of earthworm diversity (Reynolds, 1994) comprises 3627 earthworm species described worldwide, with an average annual addition of 68 species. The overall richness is expected to be at least twice this value, with the majority of still unknown species living in the tropics. For most species, the original description is the only information available, and nothing is known about their distribution, ecology, demography, physiology and resistance to disturbance. For example, on the basis of the number of native species found in two moder­ ately well sampled regions, the state of Veracruz, Mexico, 33 species (Fragoso, in press), and Puerto Rico, 18 species (Borges, 1988; Borges and Moreno, 1989, 1990a,b, 1991, 1992), it is possible to predict the possible number of native species to be found in six scarcely sampled countries: three Central American continental countries (Honduras, Nicaragua and Guatemala) and three larger Caribbean islands (Cuba, Hispaniola and Jamaica). In the first group, nearly 50 species per country should be found in the future, whereas in the second group the number of species expected to be discovered is approx­ imately ten (Jamaica), 130 (Hispaniola) and 200 (Cuba). This means that if sampling in these two regions is made with an eiTort similar to that in Veracruz and Puerto Rico, we should expect to find nearly 500 new native species in the future. Similar conclusions have been reached for Tasmania and Australia, where 150 and 600 species, respectively, are expected to be found once inventories are completed (Kingston and Dyne, 1995). This chapter is the result of a 6-year project focused on characterizing the identity of earthworms in natural and managed ecosystems of the tropics (out­ lined in Fragoso et al., 1995). The main objective was to select a group ofearth­ worm species with potential for management in tropical agroecosystems, according to the following criteria: (i) a wide distribution; (ii) with adaptations to a wide range of environmental and edaphic conditions; and (Hi) resistance to disturbances induced by agriculture. A Survey of Tropical Earthworms 3

Storage and Analysis of Data

The survey was conducted in selected regions of the tropics, and included field sampling and literature data. Most field data were obtained from the experi­ mental sites related to this project (the MACROFAUNA network, see Chapters 4 and 5). Although it was not the principal objective, this survey allowed the discovery and description of approximately 50 new species.

EWDBASE: a database of tropical earthworms

All the information was stored in a database (EWDBASE) that includes infor­ mation on the taxonomy and distribution of earthworm species, earthworm and other macroinvertebrate communities, climate of localities, edaphic and land-use variables, and socioeconomic aspects of agricultural lands where available. Inputs to EWDBASE (climatic, edaphic and species distribution data) were taken from the following published literature: Mexico, Central America and the Caribbean islands (Eisen, 1895, 1896, 1900; Michaelsen, 1900, 1908, 1911, 1912, 1923, 1935, 1936; Cognetti, 1904a,b, 1905, 1906, 1907, 1908; Pickford, 1938; Gates, 1954, 1962a,b, 1970a,b, 1971, 1972, 1973, 1977a,b, 1979, 1982; Graff, 1957; Righi, 1972; Righi and Fraile, 1987; Sims, 1987; Borges, 1988, 1994; Borges and Moreno, 1989, 1990a,b, 1991, 1992; Fraile. 1989; James, 1990, 1991, 1993; Csuzdi and Zicsi, 1991; Zicsi and Csuzdi, 1991; Fragoso, 1993, in press; Rodrfguez, 1993; Fragoso and Rojas, 1994; Reynolds and Guerra, 1994; Reynolds and Righi, 1994; Fragoso et al., 1995; Reynolds et al., 1995; Rodrfguez and Fragoso, 1995), Bolivia (Rombke and Hanagarth, 1994), Ivory Coast (Omodeo, 1958; Lavelle, 1978, 1983; Tondoh. 1994), Congo (Zicsi and Csuzdi, 1986), Ghana (Sims, 1965), Gambia (Sims, 1967), Peru (Yurimaguas; Lavelle and Pashanasi, 1988) and several regions from India (Senapati, 1980; Chaudry and Mitra, 1983; Julka, 1986, 1988; Julka and Paliwal, 1986; Julka and Senapati, 1987; Bhadauria and Ramakrishnan, 1989; Julka et al., 1989; Bano and Kale, 1991; Blanchart and Julka, 1997). EWDBASE was also fed with data obtained from field sampling carried out in Mexico, Panama, Colombia, Ivory Coast, India, Martinique, Guadaloupe, Rwanda, Peru, Congo and Cuba by members of the macrofauna network. EWDBASE included data relating to 457 species, 745 localities and 836 sites from 28 countries. Distribution and environmental plasticity were ana­ lysed by relating species distribution to climate (1310 records), soils (818 records) and types ofland use (1755 records). 4 C. Fragoso et al.

Data analysis

Data were analysed at three geographic levels, Le. local, regional and world­ wide. At the locallevel, we intended to characterize the persistence of native earthworm species in difIerent land-use systems (e.g. conversion of tropical deciduous forests to maize or pastures in Panuco, Mexico; maize plantations in native savannas of Lamto, Ivory Coast or the eastern llanos of Colombia; tea plantations in cloud forests of India, etc.). At the regionallevel, the analysis was extended to geographic areas such as southern Mexico, northern Rwanda or the Baoule region around Lamto (Ivory Coast), with the aim of identifying widespread native species. The worldwide analysis evaluated the distribution of exotic species in difIerent natural and managed tropical ecosystems. The integration ofthese data in a global analysis produced three main outputs: (i) a list of tropical species ofworldwide distribution thatcan be manipulated in any agroecosystem; (ii) regional lists of species by countries and/or kinds of agroecosystems; and (iii) an evaluation of the environmental and edaphic plasticity ofthese selected species. Earthwormspecies ofEWDBASE were classified along three difIerent axes: 1. Biogeography, to divide species depending on this origin into natives and exotics. Native earthworms are those species that evolved in the site or region under study. Exotic species are earthworms that did not originate in the site under study and that were, generally, introduced by human activities; these species have also been called peregrine (Lee, 1987) and anthropochorous (Gates, 1970c). 2. Distribution among land-use systems, to separate species on the basis of their capabilities to adapt to natural (e.g. primary forests or savannas) or managed (e.g. annual crops or pastures) systems. 3. Ecological plasticity, to rank earthworms according to their ecological tol­ erance to edaphic and environmental variables from stenoecic (narrow range) to euryoecic (wide range) species. These three axes were combined with the three geographic scales ofanaly­ sis (local,·regional and global) in order to propose the most appropiate earth­ worm species for manipulation in a given region and/or country in a specific agricultural situation.

Earthworm Species of Tropical Agroecosystems

The exotic earthworms of the tropics

Since the early studies of Eisen (1900) and Michaelsen (1903, 1935), it has been observed that peregrine worms were very common in tropical disturbed ecosystems. In a paper that analysed the distribution and dispersal of this A Survey of Tropical Earthworms 5 group of species, Lee (1987) stated that these species '... more than any others, ... are important in maintaining soil fertility in agricultural and pasto­ raI lands.' Although the author did nat present the complete list of species, he mentioned that peregrine species comprise nearly 100 species (approx. 3% of aH earthworms). Peregrine earthworms become exotics when the geographic area ofoccurrence does not correspond to the original area ofdistribution. The number ofrecords oftropical exotic species is enormous, and their dis­ tribution should be analysed using the three scales mentioned above (world­ wide, regional and local), because sorne species with wide distributions may be restricted to one kind of land-use system or have narrow climatic and edaphic niches that are not represented in a given country or continent. From EWDBA8E and a literature review (Gates, 1972,1982; Lee, 1987; Mele et al., 1995), we identified 51 exotic species commonly distributed across tropical countries (Table 1.1). Fifteen were temperate Lumbricidae of Euro­ pean origin, restricted to high altitude mountain localities. Their frequent occurrence in natural temperate forests suggests that these species may have replaced natives, as has been observed by Fragoso (in press) in the temperate forests of Veracruz, Mexico. The absence ofthis group ofexotics in low altitude tropical agroecosystems (from EWDBA8E queries) eliminates their potential for manipulation and, therefore, this group ofspecies will no longer be consid­ ered in this chapter. From Table 1.1, we selected a group of 20 species distributed worldwide, which are mainly from localities below 1000 m. This group is presented in Table 1.2, ranked according to their frequencies in agroecosystems; Table 1.3 shows, for the above group of species, the ranges of environmental (precipita­ tion and temperature) and edaphic (pH, organic matter, nitrogen, sand and clay) situations in which they occur. From the data in Tables 1.2 and 1.3, it is possible to make a preliminary separation of another group of species adapted to difIerent managed agroecosystems and with wide ranges of environmental and/or edaphic plasticity. These species include Pontoscolex corethrurus, Polypheretima elongata, Dichogaster bolaui, OcnerodriIus occidentalis, Amynthas graciIis, A. corticis, Dichogaster affinis and D. saliens, and aH of them are tolerant to very low soil concentrations ofnutrients, organic matter and nitrogen.

The widespread native earthworms of the tropics

The majority ofnative species are not very tolerant and are restricted mainly to natural environments. Of the 404 native species stored in EWDBA8E, 274 species (67%) were restricted to a single locality, whereas 207 (51%) were found exclusively in natural environments. On the other hand, nearly 40% of native species ofEWDBA8E were found inhabiting at least one of five types of agricultural land-use systems: pastures, crops, tree plantations, organic wastes and faHows (Table 1.4). Only a smaH proportion of these native species, Continued p.16 Table 1.1. The exotic earthworms of the tropics. Continental, country and altitudinal distribution.

Distribution Altitude (m) Species Family Origin Continents Countries (average) All%bophora ch/orotica Lumbricidae Europe 3 34 3000 Amynthas corticis Megascolecidae Asia 5 40 0-2500 (1243) Amynthas gracilis Megascolecidae Asia 5 31 0-2000 (962) Amynthas morrisi Megascolecidae Asia 4 23 610 Amynthas rodericensis Megascolecidae Asia 3 26 0-1200 (420) Aporrectodea ca/iginosa Lumbricidae Europe 4 15 1150-3850 (3168) Aporrectodea /onga Lumbricidae Europe 5 27 2240-2400 n Aporrectodea rosea Lumbricidae Europe 5 52 500-4650 (2972) ." Aporrectodea trapezoides Lumbricidae Europe 5 19 1200-3300 (2650) iiJ ~ 1300-3400 (2570) ln Aporrectodea turgida Lumbricidae Europe 5 20 c Bimastos parvus Lumbricidae N. America 5 32 12-1500 (756) ~ Bimastos tumidus Lumbricidae N. America 1 1 1000-1270 (1135) li> Oendrobaena octaedra Lumbricidae Europe 4 32 1200-4650 (2423) Oendrodri/us rubidus Lumbricidae Europe 5 46 950-4650 (2442) Oiachaeta thomasi Glossoscolecidae S. America 1 2 Sea level Oichogaster affinis Dichogastrini* W. Africa 4 24 0-1400 (391) Oichogaster annae Dichogastrini* W. Africa 2 5 60-1940 (1438) Oichogaster bo/aui Dichogastrini* W. Africa 5 43 0-1360 (259) Oichogaster gracilis Dichogastrini* W. Africa 2 2 Under 500 Oichogaster modigliani Dichogastrini* W. Africa 4 20 0-1100 (339) Oichogaster saliens Dichogastrini* W. Africa 4 17 0-1100 (307) Orawida barwelli Moni1igastridae India 2 11 0-1 000 (347) Eisenia fetida Lumbricidae Europe 5 45 1300-1500 (1394) Eiseniella tetraedra Lumbricidae Europe 5 45 1300-3820 (3109) Eudrilus eugeniae Eudrilidae W. Africa 4 31 0-60 (15) Eukerria kukenthali Ocnerodri1idae S. America 2 8 n.d Eukerria mcdonaldi Ocnerodrilidae S America 1 1 300 Eukerria peguana Ocnerodrilidae S. America 1 1 n.d. Eukerria saltensis Ocnerodrilidae S. America 4 10 550-3875 (1911) Eukerria zonalis Ocnerodrilidae S. America 1 1 300 Cordiodrilus peguanus Ocnerodri1idae C. Africa 4 7 n.d. Hyperiodrilus africanus Eudrilidae W. Africa 1 6 n.d. Lumbricus rubellus Lumbricidae Europe 5 34 1500-3750 (2739) ). Lumbricus castaneus Lumbricidae Europe 3 23 n.d. v., Lumbricus terrestris Lumbricidae Europe 5 36 n.d. ...,e: ~ Metapheretima taprobanae Megascolecidae Asia 4 7 10-40 (30) '<: 0 Metaphire californica Megascolecidae Asia 5 21 0-2000 (982) ...... Metaphire houlleti Megascolecidae Asia 5 20 10-853 (408) :;i Metaphire posthuma Megascolecidae Asia 2 12 12-22 (17) .g r;' Microscolex dubius Acanthodrilinae* S. America 5 16 n.d. ~

Microscolex phosphoreus Acanthodrilinae* S. America 5 28 1500-3600 (1506) [G1 Nematogenia panamaensis Ocnerodrilidae C. America 3 12 n.d. g.

Ocnerodrilus occidentalis Ocnerodrilidae C. America 5 22 0-1520 (470) ~

Octolasion cyaneum Lumbricidae Europe 5 30 1050-2430 (1576) ~ Octolasion tyrtaeum Lumbricidae Europe 5 35 1180-4654 (231 3) '" Periscolex brachycystis Glossoscolecidae C. America 1 4 0-500 (192) Peryonix excavatus Megascolecidae Asia 4 19 300-1050 (1077) Pheretima bicincta Megascolecidae Asia 3 12 30-1100 (577) Polypheretima elongata Megascolecidae Asia 4 27 0-1300 (185) Polypheretima taprobanae Megascolecidae Asia 4 7 1360 Pontoscolex corethrurus Glossoscolecidae S. America 4 56 0-2000 (463)

*Tribe or subfamily of Megascolecidae; n.d. =not determined. Table 1.2. Distribution of common exotic earthworms in different tropical land-use systems. No. of records from Mexico, Central America, the Caribbean, Colombia, Rwanda, Congo, Ivory Coast and India.

Natural Tree Species ecosystems Crops Pastures plantations Fallows Organic wastes

Pontoscolex corethrurus 94 31 44 41 6 4 Polypheretima elongata 30 10 39 19 4 5 Dichogaster bolaui 11 7 15 11 3 5 Ocnerodrilus occidentalis 3 6 15 7 2 1 Amynthas gracilis 7 4 6 9 2 2 Amynthas corticis 22 6 7 4 2 2 Hyperiodrilus africanus 2 4 8 5 1 2 !l Dichogaster affinis 9 5 5 7 1 0 ..." til Dichogaster saliens 5 1 9 4 1 0 ~

Ca Mg T Rainfall aM N (mEq (mEq S C Species (oC) (mm) pH (%) (%(x 0.1)) 100 g-l) 100 g-l) (%) (%) Pontoscolex corethrurus 14-28 268-5000 3.8-8.2 0.9-12.6 0.1-9 0.8-16.5 0.1-11.2 3-91 6-87 Polypheretima elongata 21-30 800-4000 5-7.8 1.8-7.6 0.8-3.8 4.4-53 1-2.7 5-93 4-54 Dichogaster bolaui 18-30 800-4725 5-8.2 1-10.2 0.2-8.8 1.7-44 0.06-9 5-93 4-53 Ocnerodrilus occidentalis 16-30 146-4725 5.6-8.9 0.9-7.8 0.7-8.9 0.8-53 0.06-4.5 18-98 2-74 ~ V) Amynthas gracilis 15-26 670-3500 4.8-8.9 1.7-14.4 0.7-5.9 1.3-3.4 0.7-.46 11-61 9-53 c::

Amynthas corticis 13-26 865-4521 3.9-7.5 2-12.6 2-4.2 1.9-5.8 1.5-3.5 36-61 17-33 ~ Dichogaster affinis 17-28 440-2240 4.5-8.2 1-13.7 0.7-8.8 0.82-53 0.06-4.9 9-98 2-74 '<:: 0 Dichogaster saliens 22-28 916-4725 5-8.9 0.6-6.2 0.2-8.9 0.9-12.5 0.06-4.5 18-91 6-47 .... ::;l Drawida barwelli 1500-4000 5-7.9 3.6-5.4 2-2.5 3.5-5.8 1.1-3.5 0 21-26 3-42 24-87 ~ Eudrilus eugeniae 25-28 1352-1880 n.d. n.d. n.d. n.d. n.d. n.d. n.d. Dichogaster annae 28 1880 3.7-6.3 1.6-4.9 1-2.6 n.d. n.d. 32-85 11-54 [ !i\1 Amynthas rodericensis 20-26 1200-5000 4.7-8 n.d. n.d. n.d. n.d. n.d. n.d. ::l. Peryonix excavatus 15-24 865-2173 7.1-7.5 3 n.d. n.d. n.d. 50 33 :l"" Metaphire californica 21 2631 5.2-5.6 4.3-5.4 2.2-2.5 3.5-5.8 1.5-3.5 36-42 24-28 ~

Metaphire houlleti 22-26 1314-1996 6.8 2 n.d. n.d. n.d. n.d. n.d. III3 Metapheretima taprobanae 26 1450-2000 6.4-8 n.d. n.d. n.d. n.d. n.d. n.d. Dichogaster modigliani 25 1396 n.d. n.d. n.d. n.d. n.d. n.d. n.d. Periscolex brachycystis 24-28 1880-4725 5-6.5 2.2-7.6 1.1-4.2 4.1-44 1.1-3.6 5-62 9-50 Pheretima bicincta 21-26 2500-3500 n.d. n.d. n.d. n.d. n.d. n.d. n.d. Metaphire posthuma 24 916-1079 8.1 1.2 1 6.6 0.86 46 18

T =temperature, aM =organic matter, N = nitrogen, Ca =calcium, Mg =magnesium, S =sand, C =clay; ail values from the upper 10 cm of soil. <.0 10 C. Fragoso et al.

Table 1.4. Native earthworm species of tropical agroecosystems.

Species C P T F W

Belize Diplotrema jenniferae Bolivia Andiorrhinus bolivianus Enantiodrilus borelli Eukerria asuncionis Eukerria eiseniana Eukerria garmani Eukerria tuberculatus Goiascolex vanzolinii Colombia Andiodrilus yoparensis 1 Andiorrhinus sp.nov1 1 Glossodrilus sikuani 1 1 Glossodrilus spl 1 2 2 3 Martiodrilus agricola 1 2 Martiodrilus carimaguensis 1 Martiodrilus savanicola 1 1 Martiodrilus sp1 1 3 Thamnodrilus sp1 2 Congo Dichogaster graffi Gordiodrilus sp1 Nematogenia lacuum Costa Rica Glossodrilus dorasque Glossodrilus nemoralis 4 Glossodrilus orosi 1 Cuba Diplotrema ulrici 1 Onychochaeta elegans 1 4 4 Onychochaeta windlei 2 2 3 Pontoscolex cynthiae 1 3 Zapatadrilus morenoae 1 Zapatadrilus siboney Zapatadrilus taina El Salvador Eutrigaster sporadonephra Guadaloupe Pontoscolex spiralis 2 A Survey of Tropical Earthworms 11

Table 1.4. Continued.

Species C P T FW India Curgiona narayani 3 Drawida ampullacea 1 3 1 2 Orawida assamensis 1 Drawida calebi 1 1 2 Orawida fakira 1 Orawida ferina 2 Orawida ghatensis Orawida japonica 1 Orawida kanarensis 1 Orawida lennora 1 Orawida modesta 1 Drawida nepalensis 1 2 Drawida paradoxa 1 10 Orawida pellucida 2 Orawida spl 1 Orawida sp2 1 Orawida scandens 1 Orawida sp3 4 Orawida sulcata Orawida thurstoni 4 Drawida willsi 1 3 1 Eutyphoeus festivus 2 Eutyphoeus incommodus 2 3 Eutyphoeus orientalis 1 Eutyphoeus spl Eutyphoeus waltoni Gen.nov1 sp.nov1 8 1 Gen.novl sp.nov2 2 Gen.nov2 sp.novl 1 Gen.nov3 sp.novl 3 Clyphidrilus tuberosus 2 Clyphidrilus annandalei 2 Hoplochaetella kempi 1 H. sanvordemensis Hoplochaetella suctoria Hoplochaetella spl 1 Hoplochaetella sp2 2 Karmiella kamatakensis 6 1 Karmiella spl 1 Konkadrilus sp1 6 1 1 Konkadrilus sp2 8 2 Konkadrilus tirthahalliensis 6 Lampito mauritii 3 2 5 Lennogaster chittagongensis 1

Continued 12 C. Fragoso et al.

Table 1.4. Continued.

Species C PT F W Lennogaster pusillus 3 3 Lennogaster sp1 1 Lennosco/ex sp1 1 Lennogaster dashi 2 Mallehulla indica 1 Megasco/ex fe/icisetae 1 Megasco/ex sp1 3 Megasco/ex insignis 1 1 1 Megasco/ex konkanensis 2 2 3 Megasco/ex /awsoni 2 Nellosco/ex strigosus Notosco/ex sp1 Octochaetona beatrix Octochaetona rosea Octochaetona surensis Pellogaster benga/ensis Perionyx sp1 P/utellus tumidus Ramiella bishambari Tonosco/ex horaii 2 Travoscolides duodecimalis Wahosco/ex sp1 4 Ivory Coast Agastrodrilus opisthogynus 1 Chuniodrilus palustris 10 1 1 3 Chuniodrilus zielae 10 1 1 3 Dichogaster agilis 9 1 2 2 Millsonia anoma/a 9 1 1 3 Millsonia /amtoiana 1 1 1 Millsonia sch/egeli 2 Jamaica Eutrigaster grandis Martinique Pontosco/ex cuasi 1 Pontoscolex spiralis 2 2 Mexico Ba/anteodrilus pearsei 4 10 1 2 2 Dip/ocardia eiseni 1 Dip/ocardia sp.nov1 6 Dip/ocardia sp. 1 Dip/ocardia sp.nov2 3 6 Dip/otrema sp.nov1 1 Diplotrema murchiei 1 11 3 A Survey of Tropical Earthworms 13

Table 1.4. Contin ued.

5pecies C PT FW Oiplotrema papillata 4 Gen.nov4 sp.novl 3 Gen.novS sp.novl 1 Larsonidrilus microscolecinus 2 Larsonidrilus orbiculatus 3 Lavellodrilus maya 3 Lavellodrilus parvus 5 5 1 1 Lavellodrilus riparius 1 Mayadrilus rombki Phoenicodrilus sp.novl 1 Phoenicodrilus taste 1 16 2 Protozapotecia australis 1 6 1 1 Ramiellona sp.novl 1 Ramiellona sp.nov2 Ramiellona sp.nov3 Ramiellona sp.nov4 Ramiellona sp.novS Ramiellona sp.nov6 Ramiellona sp.nov7 1 Ramiellona strigosa 1 2 Ramiellona wilsoni 1 Zapatadrilus sp.nov1 3 3 9 3 Zapotecia amecameca 1 Zapotecia nova 4 3 Zapotecia sp1 3 1 Peru Oiachaeta xepe 1 2 1 Rhinodrilus lavellei 1 1 Rhinodrilus pashanasi 1 1 1 Rwanda Oichogaster itoliensis 2 1 1 Oichogaster sp1 1 1 2 Eminoscolex lavellei 3 1 5 Gordiodrilus sp1 4 1 15 Stuhlmannia variabilis 1 2

No. of records from EWDBA5E. C=crops, P=pastures, T=tree plantations, F=fallows,W=organic wastes. Table 1.5. Environmental tolerance ranges (c1imatic and edaphic) of selected tropical native earthworms (data from EWDBASE). .l>- Ca Mg T Rainfall aM N (mEq (mEq 5 C Species (OC) (mm) pH (%) (% (x 0.1)) 100 g-l) 100 g-l) (%) (%) Cuba a. e/egans 28 1880 n.d. 7.6 n.d. 44 9 5 50 India D. ampullacea 22 5000 4.6-5.8 4.3-11 0.17-0.48 2.5-14 1-3.7 15-43 18-53 D. paradoxa 22 5000 4.4-5.1 3.6-9.3 0.19-0.33. 2.4 0.93 23 40 D. wil/sii 30-31 1150-2363 5.9-6.8 0.9-2.4 0.08-0.38 n.d. n.d. 83-95 2-7 E. incommodus 16-30 1014-1600 5.9-6.8 1-3 n.d. n.d. n.d. n.d. n.d. n D. nepa/ensis 16-26 1014-1600 6.7-6.8 1-2 n.d. n.d. n.d. n.d. n.d. ~ K. karnatakensis 22 5000 4.7-5.5 4.2-7.5 0.17-0.33 5.04 1.71 28 18-40 tU ~ L. mauritii 24-31 865-2166 6-6.7 1-3.2 0.08-0.19 n.d. n.d. 83-91 4-7 li> 0 L. pusillus 16-30 1014-1700 5.9-6.8 1-5 n.d. n.d. n.d. 47 34 !S a. beatrix 16-24 865-1314 6.8-7.1 2 n.d. n.d. n.d. n.d. n.d. ~ K. spl 22 5000 4.4-5.8 4.2-11 0.17-0.48 14.8 3.74 n.d. 18-53 K. sp2 22 5000 4.4-5.8 3.6-10.8 0.17-0.48 2.4-15 0.9-3.7 15-43 18-53 Mexico B. pearsei 24-27 916-2963 5.5-8.2 1-14.4 0.09-0.59 0.9-23 0.06-5 9-82 10-86 D. murchiei 24-27 916-2160 7.5-8.9 0.2-2.6 0.06-0.88 1.3-21 0.06-3 22-98 2-74 D. papillata 25-27 814-2130 n.d. n.d. n.d. n.d. n.d. n.d. n.d. L. parvus 24-27 1156-4725 5.3-8.1 0.9-10.1 0.07-0.42 4.5-17 0.65-11 19-63 13-74 P. taste 19-27 600-2963 5-8 1-14.4 0.08-0.42 4.1-23 0.06-6 9-78 9-86 P. australis 14-25 600-2522 5.3-7.9 1.4-11.8 0.07-0.42 5.6-14 1-6.1 11-63 12-73 R. strigosa 24-27 1000-2963 5-6.5 2.2-6.5 0.11-0.42 4.1-13 1.7-3.6 32-62 9-50 Z. sp.nov 1 24-25 916-1349 7.7-8.3 1.1-7.3 0.02-0.48 0.87-24 0.18-3 9-46 26-62 Ivory Coast C. palustris 28 1276 5-7 0.75-1.3 0.08-1.3 1.7-2.8 1-2.3 55-82 5-15 C. zielae 28 1276 5-7 0.75-1.3 0.08-1.3 1.7-2.8 1-2.3 55-82 5-15 O. agilis 28 1276 5-7 0.75-1.3 0.08-1.3 1.7-2.8 1-2.3 55-82 5-15 M. anomala 28 1276 5-7 0.75-1.3 0.08-1.3 1.7-2.8 1-2.3 55-82 5-15 Rwanda E. lavellei n.d. n.d. 3.7-7.4 1.6-4.9 0.08-0.24 n.d. n.d. 32-60 29-54 G.sp1 n.d. n.d. 3.5-7.8 1.4-41.2 0.06-1.4 n.d. n.d. 2-92 10-67 S. variabilis n.d. n.d. 3.7-4.4 3.5-4.7 0.13-0.26 n.d. n.d. 42-85 11-48

T = temperature, DM = organic matter, N = nitrogen, Ca = calcium, Mg = magnesium, 5 = sand, C = clay; ail values from the upper 10 cm of soil. 16 C. Fragoso et al. however, are common in tropical agroecosystems (Table 1.4, 31 species in bold). This group includes species widely distributed at the regionallevel (e.g. Onychochaeta elegans in Cuba, Balanteodrilus pearsei in southeastern Mexico or Lampito mauritii in India) or locally abundant (Ramiellona strigosa, Zapatadrilus sp.nov1 in Mexico and Millsonia anomala in Ivory Coast). Table 1.5 shows the environmental (precipitation, temperature) and edaphic (pH, organic matter, nitrogen, sand and clay) tolerance ranges ofsome ofthese species, according to the country in which they occur. Species listed in this table are those for which these data were available.

Comparisons between exotic and widely distributed native earthworm species

So far, we have identified 20 exotic and 27 native species thatcommonly occur in tropical agroecosystems of Asia, Arrica and America (Tables 1.2 and 1.5). Data from Tables 1.3 and 1.5 suggest that these species apparently have wide ranges of climatic and edaphic tolerances. Figure 1.1 shows that the degree of tolerance (Le. the environmental plasticity) is larger in the group of exotics, both at the regional (range of annual precipitation) and locallevel (range of pH). In this figure, however, environmental plasticity is analysed with range values (dilTerence between maximum and minimum) ofonly two variables. In order to determine whether this pattern is maintained with more variables, two multivariate analyses were performed using the climatic (two) and edaphic (seven) variables of Tables 1.3 and 1.5. The input matrix consisted of 47 rows (native and exotic species) and nine columns (environmental vari­ ables), data being standardized in both cases. The first analysis was a principal component analysis (PCA) , that ordinated species along two components which together explained 76% of the total variance (Cl = 62%, C2 = 14%). Cl and C2 correlated, respectively, with edaphic and climatic ranges. The second analysis was a cluster analysis, performed using unweighted pair-groups method analysis (UPGMA) as an average-linkage clustering method. PCA and UPGMA were made respectively, with STATGRAPHIC and PATN (Belbin, 1976) software. Figure 1.2 shows the result of these analyses that ordinated and grouped the native and exotic species listed in Tables 1.3 and 1.5, into four main groups: 1. G1 includes those native species with wide edaphic and medium climatic tolerances (high local plasticity but low regional plasticity), which correspond to the majority of native widespread Mexican species. 2. G2 are the common exotic species of the tropics that exhibit wide climatic and edaphic tolerances (high regional and local plasticity). 3. G3 includes species (natives and exotics) with narrow edaphic tolerances that are resistant to climatic variations (low local but high regional plasticity). A Survey of Tropical Earthworms 17

5 Euryoecious JI • 4 • • • J: • c- 3 • o. 0 .. '0 cP • al Cl c: al 2 a: • 0 0 • GD 00 ..-Stenoecious 0 0 • 0 0 1000 2000 3000 4000 5000 Range of precipitation (mm)

o Natives • Exotics

Fig. 1.1. Example of c1imatic (annual precipitation) and edaphic (pH) plasticity of exotic and native widespread tropical earthworm species. Each point represents a species. Those situated in the upper right corner indicate euryoecious species, whereas those situated in the lower left corner indicate stenoecious species. Both precipitation and pH are range values.

- Climatic plasticity (regional)

Stenoecious

Edaphic plasticity (local) +

+ • Exotics D Natives Fig. 1.2. Ordination (PCA) and c1ustering (UPGMA) of widespread native and exotic species on the basis of c1imatic and edaphic range values. For initiais see Table 1.6. 18 C. Fragoso et al.

4. G4 groups species with low tolerance to bothclimatic and edaphic variables (low regional and local plasticity). It is this group in which the majority of the other native species ofTable 1.4should be placed. Although this analysis is somewhat biased by the amount of records and/or data available (sorne species have very few records and consequently low ranges), the output ordination and classification is useful because it pro­ vides a framework for the classification of earthworms with potential for manipulation, according to their ecological plasticity. Thus, G2 (euryoecics) includes those exotic species that can be manipu­ lated in the majority of tropical agroecosystems, both if they are introduced and if they are already present. They represent the species best adapted to unsuitable edaphic environments: Amynthas gracilis (Ag), A. corticis (Ac), Dichogaster affinis (Da}), D. bolaui (Dbo), D. saliens (Ds), OcnerodriIus occidentalis (00), Pontoscolex corethrurus (Pc) and Polypheretima elongata (Pe). The last two species are endogeic mesohumic species (see Chapter 2 for a defmition of these terms) which, due to their abundances, cast production and burrowing activi­ ties, have important effects on soil processes. In the same way, GI (euryedaphic species) corresponds to native species that, for a given country and/or region, should be ranked frrst in manipulative practices because they represent the original adapted fauna: BalanteodriIus pearsei (Bp), LaveIIodriIus parvus (Lpa) , PhoenicodriIus taste (Pt), Diplotrema murchiei (Dm) and Protozapotecia australis (Pa) in Mexico and HyperiodriIus africanus for several African countries (this species was not analysed for plasticity, but is very common in different land-use systems). G3 (stenoedaphic species) comprises species that could be manipulated in different regions but in the same type of soil substrate, e.g. epigeic native (Drawida wiIIsii, Dw) and exotic species (Perionyx excavatus, Pex; BudriIus eugeniae, Be) on organic rich substrates. Finally, G4 (stenoecic species) represents the more local scale of management: native species that only survive in a given locality and in a given type of soil. They might be manipulated at a locallevel, provided no intensive or destruc­ tive practices are used (see Chapter 2). This is the case, for example, for sorne of the savanna species ofLamto (MiIIsonia anomala, Ma), sorne (but not all) forest species ofYurimaguas and several Indian (KonkadriIus spI and sp2, Kspl and Ksp2; Drawida ampullacea, Damp) and Mexican (Ramiellona strigosa, Rs; ZapatadriIus sp.novI, Zsp) species. In general, this analysis shows that exotic species are better adapted than natives to factors that change both at the regional--eontinentallevel (e.g. rain­ fall, temperature) and at the local level (edaphic changes); the majority of natives, on the other hand, are incapable of adapting to regional variations, but sorne species are still able to withstand variations at a more locallevel. Besides environmental plasticity, there are at least two other variables that could explain the wider distribution of exotics and the absence of native species in other regions. A Survey of Tropical Earthworms 19

1. Parthenogenetic reproduction: almost all exotic species in Table 1.2 are considered to be facultatively parthenogenetic, meaning that they may produce viable unfertilized cocoons. Native species in Table lA, on the other hand, only produce viable cocoons after fertilization (with a few exceptions such as P. taste and O. elegans). Parthenogenesis, therefore, appears to be an essential detenninant of the wide geographic distribution of exotics, as was originally proposed by Reynolds (1974) and Lee (1987). Ifmating is not oblig­ atory, one single individual (even a cocoon) may establish a new population. 2. Historical dispersal by man: the distribution of exotics has been greatly favoured by the spread ofplants worldwide and such practices as the use ofsoil as ballast, in thedays oflongseavoyages. Gates (19 72, 1982)intercepted, over several years, the worms that were introduced to the United States in pots con­ taining imported plants. He found all the exotic species ofTable 1.2 and many native species from several tropical and temperate countries; these species, of course, did nothaveanychanceto establish inNorth Americansoils, butwecan infer that, in the past, this situation occurred repeatedly, being the main cause for the presence of exotic species. In sorne cases, it is possible to relate the distribution ofsorne exotics to the origin of introduced plants. The African exotic species Gordiodrilus peguanus and Eudrilus eugeniae, for example, are present mainly in former European col­ onies (e.g. Greater Antilles; Gates, 1972) that were, in the past, dominated by an African slave population; they are not present, for example, in Mexico, Peru and other countries where this population was practically non-existent. In a number of cases, the absence of euryoecious native species in a given tropical country may, therefore, better be explained by human activities than by factors related to ecological plasticity.

Conclusions

The list of most common earthworm species of tropical agroecosystems includes a set ofeuryoecious exotic species, common in the majority of tropical countries, and native species that are common for a given country at local or regionallevels. Table 1.6 lists these species, their ecological categories and the geographic level at which management of their populations should be considered. Most species with potential for manipulation are large species, mainly mesohumic endogeics and epi-endogeics that live in the soil and ingest a mixture of soil and surface litter. These species can be considered as ecosystem engineers because they transfonn the edaphic profile through the production of casts and burrows; in this regard they are keystone species in the agroecosystem. Small polyhumic species may play a role in the system (e.g. as 'decompacting' species; see Chapter 5) but may not be crucial in the short term as their activities do not dramatically affect soil profile and other subordinated N Table 1.G. List of tropical earthworm species with potential for manipulation in annuaI cropping systems. 0

Species Ecological category Region Management

Oichogaster bolaui (Obo) Epigeic Humid tropics Worldwide Oichogaster saliens (Os) End. polyhumic Humid tropics Worldwide Oichogaster affinis (Oaf) End. polyhumic Humid tropics Worldwide Oichogaster annae (Oann) End. polyhumic Humid tropics Worldwide Orawida barwelli (Oba) End. polyhumic Humid tropics Worldwide Eudrilus eugeniae (Ee) Epigeic Humid tropics Worldwide Metapheretima taprobanae (Mt) End. mesohumic Humid tropics Worldwide Metaphire califomica (Mc) Epi-endogeic Humid tropics Worldwide Metaphire houlleti (Mh) Epi-anecic Humid tropics Worldwide 0 Metaphire posthuma (Mp) End. mesohumic Humid tropics Worldwide Ql Ocnerodrilus occidentalis (Oo) End. polyhumic Humid tropics Worldwide " ~ ln Periscolex brachycystis (Pb) End. polyhumic Humid tropics Worldwide 0 Peryonix excavatus (Pex) Epigeic Humid tropics Worldwide ....CIl Pheretima bicincta (Pbi) Epi-endogeic Humid tropics Worldwide ~ Polypheretima elongata (Pel) End. mesohumic Humid tropics Worldwide Pontoscolex corethrurus (Pc) End. mesohumic Humid tropics Worldwide Balanteodrilus pearsei (Bp) End. Poly-mes. SEMexico Regional Oiplotrema murchiei (Dm) End. Poly-mes. SEMexico Regional Phoenicodrilus taste (Pt) End. polyhumic SEMexico Regional Lavellodrilus parvus (Lpa) End. polyhumic SEMexico Regional Protozapotecia australis (Pa) End. polyhumic SEMexico Regional Eminoscolex lavellei (El) End. polyhumic Rwanda Regional Stuhlmannia variabilis (Sv) End. mesohumic Rwanda Regional Cordiodrilus spl (Cg) End. polyhumic Rwanda Regional Oichogaster itoliensis (Di) Anecic Rwanda Regional Onychochaeta elegans (Oe) End. mesohumic Cuba, Caribbean Regional Onychochaeta windelei (Ow) End. mesohumic Cuba, Caribbean Regional Pontoscolex spiralis (Ps) End. mesohumic Lower Antilles Regional Chuniodrilus zielae (Cz) End. polyhumic Lamto, Ivory Coast Regional Chuniodrilus palustris (Cp) End. polyhumic Lamto, Ivory Coast Regional Hyperiodrilus africanus (Ha) Epiendogeic Tropical Africa Regional Lampito mauritii (Lm) Anecic India, SEAsia Regional Orawida paradoxa (Opa) End. mesohumic Karnataka, India Regional Orawida ampullacea (Oamp) Endogeic Karnataka, India Regional Orawida willsii (Ow) Epianecic Karnataka, India Regional Orawida nepalensis (On) End. mesohumic Karnataka, India Regional Karmiella karnatakensis (Kk) End. poly-mes. Karnataka, India Regional Megascolex konkanensis (Mk) Endogeic Karnataka, India Regional Eutyphoeus incommodus (Ei) Anecic Northern India Regional Ramiellona strigosa (Rs) End. mesohumic Chiapas, Mexico Local Zapatadrilus sp.nov (Zsp) Endoanecic Veracruz, Mexico Local Rhinodrilus pashanasi (Rp) End. mesohumic Peru, Yurimaguas Local Millsonia anomala (Ma) End. mesohumic lamto, Ivory Coast Local Millsonia lamtoiana (M/) Anecic Lamto, Ivory Coast Local

N .... 22 C. Fragoso et al. soil organisms. This aspect, linked to the issue of the functional value of biodiversity, is considered in Chapters 4 and 5. The main conclusion of this survey is that native species are found fre­ quently in tropical agroecosystems, particularly in sorne countries (e.g. India) where apparently low-input agricultural techniques prevail (see Chapter 2 for more on this point), or in localities with low annual precipitations that do not permit the invasion of exotics (such as Mexican localities with annual precipi­ tations below 1300 mm, where the native endoanecic Zapatadrilus sp.nov1 dominates and no mesohumic exotics have been able to establish). Taking into account the fact that several native species survive in agroecosystems at a very locallevel (Table lA), the number of species to be manipulated in tropical farming systems turns out to be considerably greater than the 10-15 major exotic species identified in Table 1.1. In this regard, and at least for tropical regions, it is no longer possible to maintain Lee's (1987) statement that only exotic species are important in agriculturallands. In addition, it is highly prob­ able that the number of native species with potential for management in agroecosystems will increase as a function of the intensity of sampling effort. So far, we have presented the list ofearthworms with potential for manip­ ulation in tropical soils. In agriculturallands, however, manipulation prac­ tiees should be considered at the community level, because mixtures of species are generally more common than single species. In the next chapter, we will analyse these species assemblages in relation to their ecological and agricul­ tural determinants and potential for manipulation.

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Library of Congress Cataloging-in-Publication Data Earthworm management in tropical agroecosystems / edited by P. Lavelle, L. Brussaard and P. Hendrix. p. cm. lncludes bibliographical references and index. ISBN 0-85199-270-6 (alk. paper) 1. Earthworm culture -- Tropics. 2. Earthworms -- Ecology -- Tropics. 1. Lavelle, P. (Patrick) Il. Brussaard, L. (Lijbert) III. Hendrix, Paul F. SF597.E3E27 1999 639'.75--dc21 99-12081 OP ISBN 0 851992706

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